sign in sign up
<<
Home , Ammonitida, Ammonitina, Ammonoidea, Goniatite, Lytoceratina, Phylloceratina

Geological duration of ammonoids controlled their geographical range of distribution

Ryoji Wani Faculty of Environment and Information Sciences, Yokohama National University, Yokohama, Japan

ABSTRACT The latitudinal distributions in – ammonoids were analyzed at the level, and were compared with the hatchling sizes (i.e., ammonitella diameters) and the geological durations. The results show that (1) length of temporal ranges of ammonoids effected broader ranges of fossil distribution and paleobiogeography of ammonoids, and (2) the hatchling size was not related to the geographical range of fossil distribution of ammonoids. Reducing the influence of geological duration in this analysis implies that hatchling size was one of the controlling factors that determined the distribution of ammonoid habitats at any given period in time: ammonoids with smaller hatchling sizes tended to have broader ammonoid habitat ranges. These relationships were somewhat blurred in the Devonian, , , and , which is possibly due to (1) the course of development of a reproductive strategy with smaller hatchling sizes in the Devonian and (2) the high origination rates after the mass events.

Subjects Evolutionary Studies, Marine Biology, , Zoology Keywords , Hatchling size, Reproductive strategy, Latitudinal distribution, Habitat, Geological duration

INTRODUCTION Submitted 22 August 2017 Reproductive strategy is one of the major factors controlling the geographic distribution, Accepted 8 November 2017 evolutionary and extinction rates, and speciation in marine (Yacobucci, 2016 for Published 28 November 2017 ammonoids). Yacobucci (2016) presented a model for ammonoid speciation, based on Corresponding author Ryoji Wani, [email protected] their evolutionary characteristics, including heterochrony, homeomorphy, and a high Academic editor origination rate that is often linked to sea level cycles. In modern (, Kenneth De Baets , , and ), Villanueva et al. (2016) analyzed the hatchling Additional Information and sizes and their geographical ranges, and suggested that species of smaller hatchling Declarations can be found on size with a planktic post-embryonic mode of life have broader geographical ranges. In page 10 ammonoids, embryonic shells can be recognized by the presence of a primary constriction DOI 10.7717/peerj.4108 in the innermost (Landman, Tanabe & Shigeta, 1996; De Baets, Landman & Tanabe, Copyright 2015; and references therein). The embryonic ammonoid, which is termed ammonitella 2017 Wani (Drushchits & Khiami, 1970), consists of an initial chamber and about one Distributed under whorl from the caecum terminating at the primary constriction (Fig. 1). Most ammonoid Creative Commons CC-BY 4.0 hatchlings are thought to have had a planktic mode of life (Kulicki, 1974; Kulicki, 1979; OPEN ACCESS Kulicki, 1996; Drushchits, Doguzhayeva & Mikhaylova, 1977; Tanabe, Fukuda & Obata,

How to cite this article Wani (2017), Geological duration of ammonoids controlled their geographical range of fossil distribution. PeerJ 5:e4108; DOI 10.7717/peerj.4108 initial chamber

ammonitella diameter (=hatchling size) 0.25 mm

Figure 1 Ammonitella diameter in ammonoids. Photograph of embryonic shell of latidor- satum from Cretaceous. Arrow indicates the primary constriction. Full-size DOI: 10.7717/peerj.4108/fig-1

1980; Tanabe et al., 2001; Tanabe, Landman & Yoshioka, 2003; Landman, 1985; Tanabe & Ohtsuka, 1985; Landman, Tanabe & Shigeta, 1996; Westermann, 1996; Rouget & Neige, 2001; Ritterbush et al., 2014; De Baets, Landman & Tanabe, 2015). Therefore, a planktic mode of life at post-embryonic stages in ammonoids is expected to have had a significant impact on their geographical range (Landman, Tanabe & Shigeta, 1996; Westermann, 1996; Tajika & Wani, 2011; Ikeda & Wani, 2012; Brayard & Escarguel, 2013; Yahada & Wani, 2013; Zacaï et al., 2016). However, there has been little quantitative analysis on how hatchling size related to their geographical ranges. The purpose of this study is to evaluate the relationship between hatchling size and geographical ranges in ammonoids. Second, this study evaluates the relationship between geological duration and geographical ranges in ammonoids. This is of value because the geographical ranges of fossil marine organisms would appear to be positively correlated with geological duration (Jablonski, 1987; Miller, 1997; Liow, 2007; Foote et al., 2008). Three parameters for each species were chosen in order to examine the possible influence of hatchling size and geological duration on the geographic distribution of ammonoids, which would provide new insights into understanding the early life history and reproductive strategy in ammonoids: mean hatchling size, latitudinal geographical range, and geological

Wani (2017), PeerJ, DOI 10.7717/peerj.4108 2/14 duration. The former two parameters are similar to those used by Villanueva et al. (2016) for the analyses of modern cephalopods.

MATERIALS AND METHODS This study analyzed the relationship between latitudinal distributions and hatchling sizes in Devonian–Cretaceous ammonoids at the genus level only since the examined data set is available at this taxonomic level. A total of 223 genera (30 genera from the Devonian, 28 genera from the Carboniferous, 25 genera from the , 55 genera from the Triassic, 24 genera from the Jurassic, 61 genera from the Cretaceous) were analyzed for this study. The hatchling sizes (i.e., ammonitella diameters; Fig. 1) of the examined genera were obtained from De Baets, Landman & Tanabe (2015) (Table S1). The mean ammonitella diameter for each genus was calculated from the data of ammonitella diameters of the species of the same genus. The data of ammonitella diameters were grouped and analyzed for the aggregate Devonian–Cretaceous interval and for each constituent period (Devonian to Cretaceous). For each ammonoid genus, the geographic extent of their fossil occurrences was obtained through literature reviews (Chlupáč & Turek, 1983; Korn & Klug, 2002; Korn & Ilg, 2007; De Baets, Klug & Korn, 2009, for the Devonian; Korn & Ilg, 2007; Furnish et al., 2009, for the Carboniferous and Permian; Arkell et al., 1957; Tozer, 1981, ET Tozer, pers. comm., 1989, for the Triassic; Arkell et al., 1957; Howarth, 2013; Hoffmann, 2015, for the Jurassic; Arkell et al., 1957; Wright, Calloman & Howarth, 1996; Igolnikov, 2007, for the Cretaceous). The paleogeographic maps for each period (Scotese, 2011) were used to calculate the latitudinal ranges of the examined ammonoids. In this study, the geographical distribution of the examined genera was evaluated by latitudinal ranges, which is a similar approach taken by the analysis of modern cephalopods (Villanueva et al., 2016). The latitudinal ranges were transformed into distance (km) by applying the Haversine formula to calculate the great-circle distance between two points (mean radius of the Earth = 6,371 km): latitudinal range(◦) 2π ×(mean radius of the Earth)× . 360 The latitudinal distribution of the examined genera were analyzed with respect to the geological duration of each genus. The geological durations were obtained from the geological ages at the stage level that were adapted from those in Gradstein et al. (2012). This is because the examined data set is available at this stage level. In the case that the geological durations were significantly correlated to the latitudinal ranges of ammonoids, an index is introduced in order to reduce the influence from the geological durations of the examined ammonoids: (latitudinal range)/(geological duration). This index corresponds to the latitudinal ranges per unit of time. This index was calculated for each genus and was compared to their ammonitella diameters. Values were compared using analysis of variance (ANOVA) for the regression analyses and differences were considered significant at P < 0.05. Linear regressions (reduced major axes) were used for the graphics. The linear regressions with ANOVA are one of the most simple and basic approaches, so that this study aims to recognize principal relationships

Wani (2017), PeerJ, DOI 10.7717/peerj.4108 3/14 among the examined parameters. Linear regressions are used in similar analyses of modern cephalopods in Villanueva et al. (2016), thus the results of this study could be directly comparable to those in Villanueva et al. (2016). Fossil occurrences might be incomplete and therefore latitudinal distribution based on them as well. Species diversity among fossil invertebrates during the is known to be highly correlated with volume and area of sedimentary rocks (Raup, 1976). However, such difference of volume and area of sedimentary rocks in examined periods were not considered in this study. Furthermore, it is widely acknowledged that the analysis of comparative data from related species should be performed taking into account their phylogenetic relationships (Paradis & Claude, 2002). Such phylogenetic relationships were not taken into account in this study, because the numbers of the examined genera are not sufficient and the phylogenetic relationships in most examined genera are not clearly recognized. The 223 genera in this study represent approximately 10% of the number of genera listed in the Paleobiology Database data (approximately 2,500 genera). Analyses of modern cephalopods including approximately 13% of the total number of living species described to date (110 species of the 845 living cephalopod species), reveal a positive correlation between the hatchling sizes and geographical ranges (Villanueva et al., 2016). This percentage is comparable to that found in this study.

RESULTS Relationship between latitudinal range and ammonitella diameter The scatter diagrams for the aggregate Devonian–Cretaceous interval and each constituent period are shown in Fig. 2, which are derived from data summarized in Table 1. No relationship between latitudinal ranges and ammonitella diameters was found for the aggregate Devonian–Cretaceous interval nor for any constituent period (ANOVA, F = 0.309 and P = 0.58 Devonian–Cretaceous interval, F = 2.015 and P = 0.17 for the Devonian, F = 0.055 and P = 0.82 for the Carboniferous, F = 1.065 and P = 0.31 for the Permian, F = 0.354 and P = 0.55 for the Triassic, F = 0.691 and P = 0.41 for the Jurassic, F = 0.267 and P = 0.61 for the Cretaceous). Relationship between latitudinal range and geological duration The scatter diagrams for the aggregate Devonian–Cretaceous interval and each constituent period are shown in Fig. 3. Statistically significant relationships between latitudinal ranges and geological durations were found (ANOVA, F = 94.340 and P < 0.001 for the Devonian–Cretaceous interval, F = 7.739 and P < 0.01 for the Carboniferous, F = 8.148 and P < 0.01 for the Permian, F = 7.785 and P < 0.05 for the Jurassic, F = 36.976 and P < 0.001 for the Cretaceous). No significant correlation was found in the Devonian (F = 0.988 and P = 0.33) and Triassic (F = 1.624 and P = 0.21). Relationship between ammonitella diameter and index of latitudinal range and geological duration The scatter diagrams for the aggregate Devonian–Cretaceous interval and each constituent period are shown in Fig. 4. Statistically significant relationships between ammonitella

Wani (2017), PeerJ, DOI 10.7717/peerj.4108 4/14 20000 A 16000 E Devonian–Cretaceous 16000 N = 223 R2 = 0.001 12000 Permian N = 25 12000 2 8000 R = 0.044 8000 4000 4000 Latitudinal range (km) Latitudinal range (km)

0 0 0 1.0 2.0 3.0 4.0 5.0 6.0 7.0 0 0.5 1.0 1.5 2.0 2.5 Ammonitella diameter (mm) Ammonitella diameter (mm) 20000 B F Cretaceous 12000 16000 N = 61 2 Carboniferous R = 0.005 N = 28 12000 8000 2 R = 0.002 8000 4000 4000 Latitudinal range (km) Latitudinal range (km)

0 0 0 0.5 1.0 1.5 2.0 2.5 3.0 0 0.5 1.0 1.5 2.0 2.5 Ammonitella diameter (mm) Ammonitella diameter (mm) 20000 C G Jurassic 12000 16000 N = 24 R2 = 0.030 12000 8000

8000 Devonian 4000 N = 30 2 4000 R = 0.067 Latitudinal range (km) Latitudinal range (km)

0 0 0 0.4 0.8 1.2 1.6 0 1.0 2.0 3.0 4.0 5.0 6.0 7.0 Ammonitella diameter (mm) Ammonitella diameter (mm) D 16000 Triassic N = 55 2 12000 R = 0.007

8000

4000 Latitudinal range (km)

0 0 0.4 0.8 1.2 1.6 Ammonitella diameter (mm)

Figure 2 Scatter diagrams between latitudinal ranges and ammonitella diameters. (A) The aggregate Devonian–Cretaceous interval; (B) Cretaceous; (C) Jurassic; (D) Triassic; (E) Permian; (F) Carboniferous; (G) Devonian. Full-size DOI: 10.7717/peerj.4108/fig-2

diameter and the index of latitudinal ranges and geological durations were not found (P = 0.06, 0.54, 0.14, 0.76, 0.79, 0.98, and 0.37, for the aggregate Devonian– Cretaceous interval, Devonian, Carboniferous, Permian, Triassic, Jurassic, and Cretaceous, respectively). However, the larger indices are observed only in the smaller ammonitella diameters. In the Carboniferous, Triassic, and Jurassic, the larger indices tend to shift to the middle of the observed ranges of ammonitella diameters (Figs. 4C, 4D and 4F).

Wani (2017), PeerJ, DOI 10.7717/peerj.4108 5/14 Table 1 Statistics for examined values of genera. The data of examined genera for aggregate Devonian–Cretaceous interval and each constituent period are summarized.

No. of Ammonitella diameter (mm) Latitudinal range (km) genus Mean Median Standard Min. Max. Mean Median Standard Min. Max. deviation deviation Devonian–Cretaceous 223 0.998 0.850 0.575 0.51 6.00 7,919 7,780 4,666 556 17,782 Cretaceous 61 0.921 0.850 0.288 0.62 2.64 10,986 11,114 5,311 556 17,782 Jurassic 24 0.794 0.805 0.163 0.51 1.08 8,243 8,891 4,625 1,111 17,782 Triassic 55 0.819 0.760 0.181 0.57 1.35 5,981 5,557 4,237 1,111 15,559 Permian 25 0.922 0.880 0.299 0.66 2.16 7,757 7,780 3,895 1,111 14,448 Carboniferous 28 0.916 0.875 0.236 0.62 1.92 7,026 6,113 2,397 1,667 11,670 Devonian 30 1.787 1.421 1.178 0.73 6.00 5,946 6,668 2,860 1,111 11,114

No. of Geological duration (My) Index (latitudinal range/geological duration) (km/My) enus mean median standard min. max. mean median standard min. max. deviation deviation

Devonian– 223 15.69 12.40 13.46 2.0 67.9 856.14 501.38 982.26 41.62 5,556.93 Cretaceous Cretaceous 61 23.79 17.80 16.92 3.1 67.9 632.47 458.49 511.76 62.44 2,710.70 Jurassic 24 8.55 7.65 12.55 2.0 65.4 1,676.82 1,092.85 1,540.59 261.50 5,556.93 Triassic 55 7.53 4.50 8.33 2.2 37.6 1,308.00 715.25 1,314.86 88.67 5,556.93 Permian 25 23.17 26.60 10.48 3.5 41.9 421.85 318.30 392.45 41.62 2,102.62 Carboniferous 28 15.88 13.60 8.71 7.7 35.4 549.23 462.02 287.67 182.94 1,111.39 Devonian 30 13.48 13.30 4.30 5.0 28.8 474.33 501.38 289.54 77.72 1,587.69

DISCUSSION Controlling factors for latitudinal ranges of ammonoids The scatter diagrams between latitudinal ranges and ammonitella diameters (Fig. 2) revealed no relationship between the chosen parameters. In contrast, the hatchling sizes of modern cephalopods together with developmental modes (planktic or benthic) influence the geographical range (Villanueva et al., 2016). The evolutionary history of ammonoids is long (Devonian–Cretaceous), thus the geographical ranges of ammonoids can be considered as an accumulation of multiple geological time slices. Latitudinal ranges of ammonoids had a statistically significant positive correlation with the geological durations, except for the Devonian and Triassic (Fig. 3). These relationships show that the longer the geological duration of taxa, the broader the latitudinal ranges through ammonoid evolutionary history. Such a positive relationship is similar to those in other fossil marine organisms (e.g., gastropods, bivalves, arthropods, foraminifers, radiolarians, crinoids; Jablonski, 1987; Miller, 1997; Liow, 2007; Foote et al., 2008). Evolutionary longevity of ammonoid taxa influenced their geographical ranges of fossil distributions (Fig. 3). Figure 4 illustrates that the larger indices of the latitudinal ranges and the geological durations are observed only in the smaller ammonitella diameters. The exceptions are

Wani (2017), PeerJ, DOI 10.7717/peerj.4108 6/14 20000 A 16000 E

16000 12000 12000 8000 8000 Devonian–Cretaceous Permian N = 223 N = 25 2 4000 4000 R = 0.299 R2 = 0.212 Latitudinal range (km) P < 0.001 Latitudinal range (km) P < 0.01 0 0 0 10.0 20.0 30.0 40.0 50.0 60.0 70.0 80.0 0 10.0 20.0 30.0 40.0 Geological duration (My) Geological duration (My) 20000 B F 12000 16000

12000 8000

8000 Cretaceous Carboniferous N = 61 4000 2 N = 28 2 4000 R = 0.385 R = 0.229 Latitudinal range (km) Latitudinal range (km) P < 0.001 P < 0.01 0 0 0 10.0 20.0 30.0 40.0 50.0 60.0 70.0 80.0 0 10.0 20.0 30.0 40.0 Geological duration (My) Geological duration (My) 20000 C G 12000 16000

12000 8000 Devonian Jurassic N = 30 8000 2 N = 24 4000 R = 0.034 R2 = 0.261 Latitudinal range (km) 4000 P < 0.05 Latitudinal range (km) 0 0 0 10.0 20.0 30.0 40.0 50.0 60.0 70.0 0 10.0 20.0 30.0 Geological duration (My) Geological duration (My) Triassic 16000 D N = 55 R2 = 0.030 12000

8000

4000 Latitudinal range (km)

0 0 10.0 20.0 30.0 40.0 Geological duration (My)

Figure 3 Scatter diagrams between latitudinal ranges and geological durations of genera. (A) The ag- gregate Devonian–Cretaceous interval; (B) Cretaceous; (C) Jurassic; (D) Triassic; (E) Permian; (F) Car- boniferous; (G) Devonian. Regression lines are shown where correlations are statistically significant. Full-size DOI: 10.7717/peerj.4108/fig-3

those in the Carboniferous, Triassic, and Jurassic, in which such relationships are blurred. These tendencies in the analyses that reduce the influence by the geological durations imply that the hatchling size was one of the main controlling factors for geographical ranges in ammonoid habitats at a given geological point in time: ammonoids with smaller hatchling sizes tended to have broader geographical ranges of ammonoid habitats. Most ammonoid hatchlings are thought to have had a planktic mode of life (Kulicki, 1974; Kulicki, 1979; Kulicki, 1996; Drushchits, Doguzhayeva & Mikhaylova, 1977; Tanabe, Fukuda & Obata, 1980; Tanabe et al., 2001; Tanabe, Landman & Yoshioka, 2003; Tanabe & Ohtsuka, 1985; Landman, Tanabe & Shigeta, 1996; Westermann, 1996; Rouget & Neige,

Wani (2017), PeerJ, DOI 10.7717/peerj.4108 7/14 6000 A 2500 E Devonian–Cretaceous 5000 N = 223 2000 2 4000 R = 0.016 1500 Permian 3000 N = 25 1000 2 2000 R = 0.004

1000 500 Index (latitudinal range/ Index (latitudinal range/ geological duration) (km/My) geological duration) (km/My) 0 0 0 1.0 2.0 3.0 4.0 5.0 6.0 7.0 0 0.5 1.0 1.5 2.0 2.5 Ammonitella diameter (mm) Ammonitella diameter (mm) 3000 B 1200 F Cretaceous N = 61 2 Carboniferous 2000 R = 0.013 800 N = 28 R2 = 0.080

1000 400 Index (latitudinal range/ Index (latitudinal range/ geological duration) (km/My) geological duration) (km/My) 0 0 0 0.5 1.0 1.5 2.0 2.5 3.0 0 0.5 1.0 1.5 2.0 2.5 Ammonitella diameter (mm) Ammonitella diameter (mm) 6000 C G 1600 5000 Jurassic Devonian N = 24 N = 30 4000 R2 = 0.00002 1200 R2 = 0.013

3000 800 2000 400 1000 Index (latitudinal range/ Index (latitudinal range/ geological duration) (km/My) geological duration) (km/My) 0 0 0 0.4 0.8 1.2 1.6 0 1.0 2.0 3.0 4.0 5.0 6.0 7.0 Ammonitella diameter (mm) Ammonitella diameter (mm) 6000 D Triassic 5000 N = 55 2 4000 R = 0.001

3000

2000

1000 Index (latitudinal range/

geological duration) (km/My) 0 0 0.4 0.8 1.2 1.6 Ammonitella diameter (mm)

Figure 4 Scatter diagrams between index of latitudinal ranges and geological durations and ammonitella diameters. (A) The aggregate Devonian–Cretaceous interval; (B) Cretaceous; (C) Jurassic; (D) Triassic; (E) Permian; (F) Carboniferous; (G) Devonian. Full-size DOI: 10.7717/peerj.4108/fig-4

2001; De Baets, Landman & Tanabe, 2015). In modern cephalopods, hatchlings smaller than approximately 3 mm are considered to have a planktic habit in the post-embryonic stages (Wani, 2011; De Baets et al., 2012; De Baets, Landman & Tanabe, 2015; Villanueva et al., 2016), which also suggests a planktic mode of life in most ammonoids. A planktic mode of life at the post-embryonic stage is thought to have had a significant impact on their geographical ranges (Landman, Tanabe & Shigeta, 1996; Westermann, 1996; Tajika & Wani, 2011; Ikeda & Wani, 2012; Brayard & Escarguel, 2013; Yahada & Wani, 2013; De Baets, Landman & Tanabe, 2015; Zacaï et al., 2016). However, there has been little discussion of how the hatchling sizes are related to their geographical ranges. The analyses that reduce the influence of geological duration in this study imply that the

Wani (2017), PeerJ, DOI 10.7717/peerj.4108 8/14 hatchling sizes were of importance to the geographical ranges of ammonoid habitats at each geological point in time, similar to those in modern cephalopods. This similarity to modern cephalopods shows a common reproductive strategy in ancient and modern cephalopods: the planktic mode of life at the post-embryonic stages was important in order to achieve wide geographic ranges. Taxonomic treatment of ammonoid genera could also affect the geographical range and geological duration of the examined genus depending on how the examined species are attributed to a given genus. For example, Maeda (1993) examined ‘‘four’’ species of ‘‘two’’ genera of Late Cretaceous ammonoids and suggested that the examined nominal species was one species (i.e., one genus), based on the stratigraphic occurrence, morphological variation, and shell ontogeny. Such integration and separation of a genus would influence the geographical range and geological duration, the averages of ammonitella diameters, which impact analyses such as this study. Comparison between different periods The examination of the scatter diagrams for each period (Figs. 2–4) illustrates the characteristics of the relationship between the hatchling sizes and geographical ranges for each period. Scatter diagrams for the Permian and Cretaceous data demonstrate the same tendency as data for the aggregate Devonian–Cretaceous interval. But scatter diagrams of the Devonian, Carboniferous, Triassic, and Jurassic (Figs. 2–4) demonstrate different tendencies. The ammonitella diameters in the Devonian tend to be larger than found in other periods and the maximum ammonitella diameter within the Devonian attained at least 6.0 mm (Table 1; De Baets, Landman & Tanabe, 2015). Several genera had ammonitella diameters larger than 3 mm, which is thought to be the approximated critical size for the planktic habit of the post-embryonic stage in modern cephalopods (Wani, 2011; De Baets et al., 2012; De Baets, Landman & Tanabe, 2015). De Baets, Landman & Tanabe (2015) mentioned a trend towards smaller ammonitella diameters from the Early to Late Devonian: the maximum ammonitella diameters were more than 3 mm in the Early Devonian, and less than 3 mm in the Late Devonian. This implies that ammonoids developed a reproductive strategy with smaller hatchling sizes during the Devonian, which possibly blurs the relationship between the latitudinal ranges, ammonitella diameters, and geological durations in the Devonian, at the examined temporal resolution (Fig. 3). Laptikhovsky, Nikolaeva & Rogov (2017) also concluded that the of reproductive strategies in cephalopods in the geological past was marked by an increasing abundance of small-egged taxa, which agrees with the findings in this study. The scatter diagram between the latitudinal ranges and geological durations in the Jurassic (Fig. 3C) shows a significant relationship. If only one long-ranged genus ( of ) is excluded from the analyses, the scatter diagram showed no statistically significant correlation (F = 3.253 and P = 0.09). Such long-ranged genera are few in the examined data set and might indicate a possible problem with species determination; most ammonoid genera in the Triassic and Jurassic have shorter geological durations (Table 1; Table S1) (see Korn & De Baets, 2015, for a similar bias on the paleogeography of Devonian

Wani (2017), PeerJ, DOI 10.7717/peerj.4108 9/14 ammonoids). The larger indices of the geographical ranges and geological durations are observed not only in the smaller ammonitella diameters but also in the middle of the observed ranges of ammonitella diameters (Figs. 4C and 4D). Based on these values, the relationships between the hatchling diameters, geological duration, and geographical ranges in the Triassic and Jurassic are regarded as similar. There were mass extinction events at the end of the Permian and Triassic when drastic taxonomic turnovers of ammonoid fauna occurred (e.g., House, 1988; Monnet, Brayard & Brosse, 2015; Brayard & Bucher, 2015; Longridge & Smith, 2015). In the and , origination rates of ammonoids were high ( originated in the Triassic and and originated in the Jurassic; Neige & Rouget, 2015; Yacobucci, 2015; Longridge & Smith, 2015), which probably indicate radiations into open niche followed mass extinction events. At these times, ammonoids appear to have originated and resulted in an increased diversity rather than an increased geographical spread of each taxa (with the exception of some long-ranged taxa). This could blur the relationship between latitudinal ranges, geological durations, and ammonitella diameters in the Triassic and Jurassic (Figs. 2–4). There was also a mass at the end of the Devonian, after which ammonoid diversity increased during the Carboniferous (Kullmann, 1981; Becker & Kullmann, 1996; Korn, Klug & Walton, 2015). As with the Triassic and Jurassic, originations following mass extinction events, those during the Carboniferous might influence the relationship between latitudinal ranges, geological durations, and ammonitella diameters. This is possibly seen in Fig. 4F where the larger indices tend to shift to the middle of the observed range of ammonitella diameters. A more complete and detailed dataset of geographical range and geological duration with larger data size, together with the paleobiogeography of each period and morphological changes at the embryonic and post-embryonic stage, would allow us to analyze with more elaborate approaches and therefore to better understand the geological transition of ammonoid reproductive strategies during the Devonian–Cretaceous with finer geological resolution (i.e., at the stage level) and on a lower taxonomic level (i.e., at the species level).

ACKNOWLEDGEMENTS I am sincerely grateful to Amane Tajika (Universität Zürich) for his constructive suggestion and critical reading on an early manuscript, and to Kenji Ikuno (Museum of Nature and Human Activities, Hyogo and Tetsuro Iwasaki (Yokohama National University) for their help for literature reviews. I thank Kenneth De Baets, Christian Klug, and anonymous reviewers for their valuable and thoughtful comments and suggestions on an earlier draft of the manuscript.

ADDITIONAL INFORMATION AND DECLARATIONS

Funding The authors received no funding for this work.

Wani (2017), PeerJ, DOI 10.7717/peerj.4108 10/14 Competing Interests The authors declare there are no competing interests. Author Contributions • Ryoji Wani conceived and designed the experiments, performed the experiments, analyzed the data, contributed reagents/materials/analysis tools, wrote the paper, prepared figures and/or tables, reviewed drafts of the paper. Data Availability The following information was supplied regarding data availability: The raw data is included as Table S1. Supplemental Information Supplemental information for this article can be found online at http://dx.doi.org/10.7717/ peerj.4108#supplemental-information.

REFERENCES Arkell WJ, Furnish WM, Kummel B, Miller AK, Moore RC, Schindewolf OH, Sylvester- Bradley PC, Wright CW. 1957. Treatise on invertebrate paleontology part L, 4. Lawrence: Geological Society of America and University of Kansas Press. Becker RT, Kullmann J. 1996. ammonoids in space and time.. In: Landman NH, Tanabe K, Davis RA, eds. Ammonoid paleobiology. New York: Plenum Press, 711–753. Brayard A, Bucher H. 2015. Permian-Triassic and rediversifications.. In: Klug C, Korn D, De Baets K, Kruta I, Mapes RH, eds. Ammonoid paleobiology, from macroevolution to paleogeography. Amsterdam: Springer, 465–473. Brayard A, Escarguel G. 2013. Untangling phylogenetic, geometric and ornamental imprints on Early Triassic ammonoid biogeography: a similarity-distance decay study. Lethaia 46:19–33 DOI 10.1111/j.1502-3931.2012.00317.x. Chlupáč I, Turek V. 1983. Devonian from the Barrandian area, Czechoslo- vakia. Rozpravy Ústředního Ústavu Geologického 46:1–159. De Baets K, Klug C, Korn D. 2009. Anetoceratinae (Ammonoidea, Early De- vonian) from the Eifel and Harz Mountains (Germany), with a revision of their genera. Neues Jahrbuch für Geologie und Paläontologie 252:361–376 DOI 10.1127/0077-7749/2009/0252-0361. De Baets K, Klug C, Korn D, Landman NH. 2012. Early evolutionary trends in am- monoid embryonic development. Evolution 66:1788–1806 DOI 10.1111/j.1558-5646.2011.01567.x. De Baets K, Landman NH, Tanabe K. 2015. Ammonoid embryonic development. In: Klug C, Korn D, De Baets K, Kruta I, Mapes RN, eds. Ammonoid Paleobiology, From Anatomy to Ecology. Amsterdam: Springer, 113–205. Drushchits VV, Doguzhayeva LA, Mikhaylova IA. 1977. The structure of the am- monitella and the direct development of ammonites. Paleontological Journal 1977:188–199.

Wani (2017), PeerJ, DOI 10.7717/peerj.4108 11/14 Drushchits VV, Khiami N. 1970. Structure of the septa, walls and initial whorls in ammonites. Paleontological Journal 4:26–38. Foote M, Crampton JS, Beu AG, Cooper RA. 2008. On the bidirectional relationship between geographic range and taxonomic duration. Paleobiology 34:421–433 DOI 10.1666/08023.1. Furnish W, Glenister BF, Kullmann J, Zuren Z. 2009. Treatise on invertebrate paleontol- ogy part L, mollusca 4 revised. Vol. 2. Lawrence: Geological Society of America and University of Kansas Press. Gradstein FM, Ogg JG, Schmitz MD, Ogg GM. 2012. The 2012. Amsterdam: Elsevier. Hoffmann R. 2015. Treatise online, number 70, part L, revised. Vol. 3B. Lawrence: Geological Society of America and University of Kansas Press, Chapter 3. House MR. 1988. Major features of cephalopod evolution. In: Wiedmann J, Kullmann J, eds. Cephapods present and past. Stuttgart: Schweizerbart’sche Verlagsbuchhandlung 1–16. Howarth MK. 2013. Treatise online, number 57, part L, revised. Vol. 3B. Lawrence: Geological Society of America and University of Kansas Press, Chapter 4. Igolnikov AE. 2007. A new species of the genus Boreophylloceras Alekseev et Repin, 1998 () from the kochi Zone of north-central Siberia. Paleontological Journal 41:128–131 DOI 10.1134/S0031030107020037. Ikeda Y, Wani R. 2012. Different modes of migration among Late Cretaceous am- monoids in northwestern Hokkaido, Japan: evidence from the analyses of shell whorls. Journal of Paleontology 86:605–615 DOI 10.1666/11-089R.1. Jablonski D. 1987. Heritability at the species level: analysis of geographic ranges of Cretaceous mollusks. Science 238:360–363 DOI 10.1126/science.238.4825.360. Korn D, De Baets K. 2015. Biogeography of Paleozoic ammonoids. In: Klug C, Korn D, De Baets K, Kruta I, Mapes RH, eds. Ammonoid paleobiology, from macroevolution to paleogeography. Amsterdam: Springer, 145–161. Korn D, Ilg A. 2007. AMMON. Available at www.wahre-staerke.com/ammon/. Korn D, Klug C. 2002. Fossilium catalogus animalia. Pars 138. Ammoneae Devonicae. Leiden: Backhuys Publishers. Korn D, Klug C, Walton SA. 2015. Taxonomic diversity and morphological disparity of Paleozoic ammonoids. In: Klug C, Korn D, De Baets K, Kruta I, Mapes RH, eds. Ammonoid paleobiology, from macroevolution to paleogeography. Amsterdam: Springer, 431–464. Kulicki C. 1974. Remarks on the embryogeny and postembryonal development of ammonites. Acta Palaeontologica Polonica 19:201–224. Kulicki C. 1979. The ammonite shell: its structure, development and biological signifi- cance. Palaeontologia Polonica 39:97–142. Kulicki C. 1996. Ammonoid shell microstructure. In: Landman NH, Tanabe K, Davis RA, eds. Ammonoid paleobiology. New York: Plenum Press, 65–101.

Wani (2017), PeerJ, DOI 10.7717/peerj.4108 12/14 Kullmann J. 1981. Carboniferous goniatites. In: House MR, Senior JR, eds. The ammonoidea. Systematics association special volume no 18, London: Academic Press, 37–48. Landman NH. 1985. Preserved ammonitellas of (Ammonidea, ). American Museum Novitates 2815:1–10. Landman NH, Tanabe K, Shigeta Y. 1996. Ammonoid embryonic development. In: Landman NH, Tanabe K, Davis RA, eds. Ammonoid paleobiology. New York: Plenum Press, 343–405. Laptikhovsky V, Nikolaeva S, Rogov M. 2017. Cephalopod embryonic shells as a tool to reconstruct reproductive strategies in extinct taxa. Biological Reviews Epub ahead of print May 30 2017 DOI 10.1111/brv.12341. Liow LH. 2007. Does versatility as measured by geographic range, bathymetric range and morphological variability contribute to taxon longevity? Global Ecology and Biogeography 16:117–128 DOI 10.1111/j.1466-8238.2006.00269.x. Longridge LM, Smith PL. 2015. Ammonoids at the Triassic-Jurassic transition: pulling back from the edge of extinction. In: Klug C, Korn D, De Baets K, Kruta I, Mapes RH, eds. Ammonoid paleobiology, from macroevolution to paleogeography. Amster- dam: Springer, 475–496. Maeda H. 1993. Dimorphism of Late Cretaceous false-puzosiine ammonites, Yokoyamao- ceras Wright and Matsumoto, 1954 and Neopuzosia Matsumoto, 1954. Transactions and Proceedings of the Paleontological Society of Japan, New Series 169:97–128 DOI 10.14825/prpsj1951.1993.169_97. Miller AI. 1997. A new look at age and area: the geographic and environmental ex- pansion of genera during the Radiation. Paleobiology 23:410–419 DOI 10.1017/S0094837300019813. Monnet C, Brayard A, Brosse M. 2015. Evolutionary trends of Triassic ammonoids.. In: Klug C, Korn D, De Baets K, Kruta I, Mapes RH, eds. Ammonoid paleobiology, from macroevolution to paleogeography. Amsterdam: Springer, 25–50. Neige P, Rouget I. 2015. Evolutionary trends within Jurassic ammonoids. In: Klug C, Korn D, De Baets K, Kruta I, Mapes RH, eds. Ammonoid paleobiology, from macroevolution to paleogeography. Amsterdam: Springer, 51–66. Paradis E, Claude J. 2002. Analysis of comparative data using generalized estimating equations. Journal of Theoretical Biology 218:175–185 DOI 10.1006/jtbi.2002.3066. Raup DM. 1976. Species diversity in the Phanerozoic: an interpretation. Paleobiology 2:289–297 DOI 10.1017/S0094837300004929. Ritterbush KA, Hoffmann R, Lukeneder A, De Baets K. 2014. Pelagic palaeoecology: the importance of recent constraints on ammonoids palaeobiology and life history. Journal of Zoology 292:229–241 DOI 10.1111/jzo.12118. Rouget I, Neige P. 2001. Embryonic ammonoid shell features: intraspecific variation revised. Palaeontology 44:53–64 DOI 10.1111/1475-4983.00169. Scotese CR. 2011. Atlas of Earth History. Texas: PALEOMAP Project.

Wani (2017), PeerJ, DOI 10.7717/peerj.4108 13/14 Tajika A, Wani R. 2011. Intraspecific variation of hatchling size in Late Cretaceous ammonoids from Hokkaido, Japan: implication for planktic duration at early ontogenetic stage. Lethaia 44:287–298 DOI 10.1111/j.1502-3931.2010.00242.x. Tanabe K, Fukuda Y, Obata I. 1980. Ontogenetic development and functional morphol- ogy in the early growth stages of three Cretaceous ammonites. Bulletin of National Science Museum, Series C 6:9–26. Tanabe K, Kulicki C, Landman NH, Mapes RH. 2001. External shell features of embry- onic and early postembryonic shells of a Carboniferous Vidrioceras from Kansas. Paleontological Research 5:13–19 DOI 10.2517/prpsj.5.13. Tanabe K, Landman NH, Yoshioka Y. 2003. Intra-and interspecific variation in the early internal shell features of some Cretaceous ammonoids. Journal of Paleontology 77:876–887 DOI 10.1017/S0022336000044735. Tanabe K, Ohtsuka Y. 1985. Ammonoid early internal shell structure: its bearing on early life history. Paleobiology 11:310–322 DOI 10.1017/S0094837300011611. Tozer ET. 1981. Triassic Ammonoidea: classification, evolution and relationship with Permian and Jurassic forms. In: House MR, Senior JR, eds. The ammonoidea. Systematics association special volume no 18, London: Academic Press, 65–100. Villanueva R, Vidal EAG, Fernández-Álvarez FÁ, Nabhitabhata J. 2016. Early mode of life and hatchling size in cephalopod molluscs: influence of the species distributional ranges. PLOS ONE DOI 10.1371/journal.prone.0165334. Wani R. 2011. Sympatric speciation drove the macroevolution of fossil cephalopods. Geology 39:1079–1082 DOI 10.1130/G32317.1. Westermann GEG. 1996. Ammonoid life and habitat. In: Landman NH, Tanabem K, Davis RA, eds. Ammonoid paleobiology. New York: Plenum Press, 607–707. Wright CW, Calloman JH, Howarth MK. 1996. Treatise on invertebrate paleontology part L, mollusca 4 revised. Vol. 4. Lawrence: Geological Society of America and University of Kansas Press. Yacobucci MM. 2015. Macroevolution and paleobiogeography of Jurassic-Cretaceous ammonoids.. In: Klug C, Korn D, De Baets K, Kruta I, Mapes RH, eds. Ammonoid paleobiology, from macroevolution to paleogeography. Amsterdam: Springer, 189–228. Yacobucci MM. 2016. Towards a model for speciation in ammoniods.. In: Allmon WD, Yacobucci MM, eds. Species and speciation in the fossil record. Chicago: University of Chicago Press, 238–277. Yahada H, Wani R. 2013. Limited migration of scaphitid ammonoids: evidence from the analyses of shell whorls. Journal of Paleontology 87:406–412 DOI 10.1666/12-077.1. Zacaï A, Brayard A, Dommergues J-L, Meister C, Escarguel G, Laffont R, Vrielynck B, Fara E. 2016. Gauging scale effects and biogeographical signals in similarity distance decay analyses: an Early Jurassic ammonite case study. Palaeontology 59:671–687 DOI 10.1111/pala.12250.

Wani (2017), PeerJ, DOI 10.7717/peerj.4108 14/14